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Glycobiology Pages 979-984  

God must love galectins; He made so many of them2
Introduction
Galectin family features
Novel candidate galectins
Evidence for multiple galectin functions
Acknowledgments
References

God must love galectins; He made so many of them<sup>2</sup>

God must love galectins; He made so many of them2

Douglas N.W. Cooper1 and Samuel H. Barondes

Center for Neurobiology and Psychiatry, Langley Porter Psychiatric Institute, University of California, San Francisco, 401 Parnassus Avenue, San Francisco, CA 94143-0984, USA

Received on April 12, 1999; accepted on April 12, 1999

Key words: galectin/lectin/review

Introduction

Galectins are a family of proteins first identified as galactoside-binding lectins in extracts of vertebrate tissue (Barondes et al., 1994a; Various authors, 1997). Sequencing of such proteins isolated from amphibians, birds, fish, and mammals revealed extensive sequence similarity, and in 1994, the galectin family was formally defined (Barondes et al., 1994b) on the basis of both shared sequence and galactoside binding. Four human galectins, which had been discovered in various contexts, and which bore multiple names, were renamed galectin-1 through -4. Since that time, advances in molecular genetics have led to the identification of many new members of the galectin gene family, which have been discovered on the basis of sequence similarity. Here we call attention to these newly established galectins and to additional genes, whose sequence suggests that they too are galectin family members.

Galectin family features

All galectins share a core sequence consisting of about 130 amino acids, many of which are highly conserved. Crystallography has been used to determine the structure of several galectins, most recently for galectin-7 (Leonidas et al., 1998). The portion of the core sequence which represents the carbohydrate recognition domain (CRD) (Figure 1) is contained between about residues 30 and 90, a segment generally encoded by a single exon. Of the original mammalian members, galectins 1-3 include just one CRD, whereas galectin-4 is composed of two nonidentical tandem core structures with two separate CRDs. Another shared feature was surprising: although galectins are found both in the cytoplasm and extracellularly, none has a secretion signal peptide. Instead, several galectins have been shown to be secreted by an unorthodox mechanism (Hughes, 1997).

Since the formal naming of the galectin family, seven more mammalian galectins (-5 through -11) have been discovered (Table I), sharing the basic structural features and galactoside-binding of the original four. Four of these have one CRD (Ackerman et al., 1993; Gitt et al., 1995; Magnaldo et al., 1995; Madsen et al., 1995; Ogden et al., 1998), and the other three have two tandem CRDs (Hadari et al., 1995; Leal-Pinto et al., 1997; Tureci et al., 1997; Wada and Kanwar, 1997; Gitt et al., 1998; Matsumoto et al., 1998) like galectin-4. Unlike the original members of this family, which were discovered on the basis of their lectin activity, the new galectins have primarily been identified in other ways, even in multiple contexts. Only when sequenced were they found to be members of the galectin family.

For one of these galectins, an apparent lack of carbohydrate binding activity resulted in its initial exclusion from the galectin family. The Charcot-Leyden crystal protein, an abundant lysophospholipase of eosinophils, could only be named galectin-10 after it was shown to weakly bind to the same galactoside affinity columns that avidly bound other galectins (Leonidas et al., 1995).

A galectin-like protein apparently specific to the lens of the eye, GRIFIN (galectin-related interfiber protein), was recently discovered, but this candidate can not be numbered as an official galectin, because it does not have detectable lectin activity in assays standardly used for other galectins (Ogden et al., 1998).

Novel candidate galectins

Using search algorithms based on the structure of these known galectins, we have screened the GenBank databases and identified seven additional mammalian candidates for membership in this family (Figure 1; only the exon-II encoded CRD domains are shown, but there is also considerable sequence similarity in other parts of each protein). All but one of these sequences (AC005515-II) appears not only in human genomic DNA, but also in expressed messages (Table I), proving that they are not pseudogenes. Based on sequence comparison it seems quite likely that most of these galectin-like sequences have galactoside-binding activity, but one (N90645) lacks the tryptophan residue otherwise conserved in all galectins with established carbohydrate binding activity. Four of the novel candidate galectins (N30757, R31311, AI138230, and AC005515-II) are also candidates for lysophospholipase activity, because they are very similar in sequence to galectin-10 (also located close to the galectin-10 gene on chromosome 19q13.1). Two additional sequences like galectin-10 appear to have stop codons interrupting the CRD. One of these appears to be expressed (EST = N40740), but no cDNA sequence has yet been recorded for the other gene. We have established a web address (URL: http://www.sacs.ucsf.edu/home/cooper/galectins.htm) giving further documentation for each of these candidate galectins, including complete deduced protein sequence.


Figure 1. Amino acid sequences of galectin CRDs are aligned to maximize sequence similarity, allowing variation in the size of some loops between [beta] strands. Highly conserved residues (specific amino acids or certain limited sets of similar amino acids) are capitalized with the most highly conserved residues also shaded. Beta strand positions are indicated at the top, with residues known to directly interact with carbohydrate marked by asterisks. Candidate galectin genes (i.e., not yet shown to bind galactosides) are indicated by an asterisk preceding their GenBank accession number. The mammalian galectins and candidates are all human, except for rat galectin-5 and mouse galectin-6. Further documentation for each of these genes is available at URL: http://www.sacs.ucsf.edu/home/cooper/galectins.htm.

Similar hunting for novel galectins in other genomes is also productive. In the worm, Caenorhabditis elegans, two galectins have been isolated and shown to bind galactosides (Hirabayashi et al., 1996; Arata et al., 1997). By searching the GenBank databases we have identified 26 more candidate galectin genes (not shown) for a tentative total of 28 galectins among the ~20,000 genes in the C.elegans genome. Candidate galectins are also apparent in the genomes of other important model organisms (Table II), including Drosophila (LP06039), zebrafish (AI384777 and G47571), and Arabadopsis (AC000348, T7N9.14). The galectin-like sequence in Arabadopsis represents the first evidence for galectins in plants, where the whole class of lectin proteins was first discovered. Candidate galectin genes are even evident in two viruses, an adenovirus (Perillo et al., 1998; U25120) and a lymphocystis disease virus (L63545, 26549-27313 = 053R).

Table I. Mammalian galectin and candidate genes
Galectin Gene Message Structure
1 22q13.1: gene J05303 CommonUnigene HS.129924 1 CRD, dimer
cosmid Z83844*    
   49650-49659    
   50934-51010    
   52430-52603    
   53552-53695    
2 22q13.1: gene M87860 IntestineUnigene HS.13987ESTs: gall bladder, kidney 1 CRD, dimer
cosmid AL022315*    
   86175-86169    
   78200-78120    
   77006-76846    
   76682-76536    
3 14q21.3: gene AF 031421-5 Common Unigene HS.621 1 CRD+N-term repet.
sts G22378    
4 19q13.1-13.3 Intestine, esp. colon Unigene HS.5302 2 CRDs
5 Human not yet identified, rat gene L36862 Rat erythrocytes 1 CRD, monomer
6 Human not yet identified mouse gene tandem to gene for galectin-4 Intestine 2 CRDs
7 19q13.1 Stratified epithelia Unigene HS.99923 1 CRD, monomer
sts G38734    
8 1q41-44 Common Unigene HS.4082 2 CRDs
stsG22174    
9 Human not yet mapped,mouse chr. 11 sts Z36627 Lymphocytes, intestine specific isoform Unigene HS.81337 2 CRDs
10 19q13.1: gene U68398 Granulocytes Unigene HS.889 1 CRD, dimer
cosmid AC005393    
   17049-17035    
   14171-14095    
   13591-13381    
   10598-10473    
Candidate Gene Message Structure
GRIFIN 7 Rat lens 1 CRD, dimer
Cosmid AC004840    
   118481-118470    
   118100-118018    
   117926-117768    
   117407-117241    
   116973-116985    
AA311108 11q23 ESTs: breast, infant adrenal, Jurkat T-cell 1 CRD
Cosmid U73641    
   28867-28853    
   28206-28120    
   24394-24242    
   23714-23568    
H50956 11q23 ESTs: spleen, gastriccarcinoma, Jurkat T-cell 1 CRD
Cosmid U73641    
   33498-33427    
   31401-31315    
   31181-30963    
   30179-30060    
   29969-29972    
N90645 2p Unigene HS.114771 ESTs: fetal heart, fetal liver/spleen 1 CRD?
sts G30627    
N30757 19q13.1 Unigene HS.24236 ESTs: placenta, aorta, embryo, fetal liver/spleen 1 CRD
Cosmid AC006133    
   ????-8278    
   10331-10398    
   10913-11123    
   12932-13303    
R31311 19q13.1 Unigene HS.23671 ESTS: placenta, fetal liver/spleen 1 CRD
Cosmid AC005205    
   14526-14541    
   16559-16633    
   17136-17348    
   19180-19293    
AI138230 19q13.1 Unigene HS.143557 EST AI138230, placenta EST AI148582, placenta 1 CRD
Cosmid AC005515    
   3464-3468    
   3925-4001    
   4502-4712    
   6437-6559    
AC005515-II 19q13.1   1 CRD
Cosmid AC005515    
   26891-26896    
   27476-27551    
   28040-28172    
   30073-30186    
Mouse gene U67985    
N40740 19q13.1 Unigene HS.146477 EST N40740, placenta EST AI128445, placenta 1 interrupted CRD
Cosmid AC005176    
   22584-22658    
   23164-23374    
Cosmid AC005515    
   1866-18989    
AC000052 22q11.2   1 interrupted CRD
Cosmid AC000052*    
   41727-42113    
*Sequencing of cosmids still in progress, so position numbering for the deduced exon boundaries may change with each update.

Table II. Nonmammalian galectin and candidate genes
Galectin Gene or message Structure
Amphibian
   Xenopus laevis M88105 1 CRD, dimer
   Bufo arenarum P56217 1 CRD, dimer
Fish
   Electrophorus electricus A28302 1 CRD, dimer
   Conger myriater Con I AB010276 1 CRD, dimer
Con II AB010277 1 CRD, dimer
   Danio rerio   *G47571 1 CRD
Gal-3 ? *AI384777 1 CRD + N-terminal Pro/Gly rich repeat
   Fugu rubripes   *FRa073apsB12 1 CRD
  *FRa075apsH3 1 CRD
Gal-3 ? *AL020875: 199D14, 111H07 1 CRD + N-terminal Pro/Gly rich repeat
Bird
   Gallus gallus C-14 D00308-11, M11674 1 CRD, monomer
C-16 M57240 1 CRD, dimer
Gal-3 ? *U50339 1 CRD + N-term. Pro/Gly rich repeat
Insect
   Anopheles gambiae Z69982 1 CRD
   Drosophila melanogaster *LP06039.5prime 1 CRD
Worm
   Caenorhabditis elegans 16 D63575; cosmid Y55B1 on ch.III-28-26 1 CRD, dimer
32 AB000802; cosmid Z82081, ch. II 7753-7767, alt. splices = W09H1.6a,6b =yk148a7.5, yk469b7.5 2 CRDs
Sponge
   Geodia cydonium I X93925 1 CRD, multimer
II X70849 1 CRD, multimer
Fungus
   Coprinus cinerea CGL-I L03301 1 CRD, dimer
CGL-II U64676 1 CRD, dimer
Virus
   Mastadenovirus *U25120 2 CRDs
   Lymphocystis disease *L63545 26549-27313 = 053R 1 CRD
Plant
   Arabadopsis thaliana *AC000348: T7N9.14 1 CRD

*Candidate galectins (not yet shown to bind galactosides). Not included are numerous candidate nematode galectins (C.elegans and others).

Evidence for multiple galectin functions

The presence of galectins in so many evolutionarily divergent species suggests that they participate in basic cellular functions. On the other hand, the evidence that there may be dozens of galectins within a single species suggests that they have evolved to participate in a variety of more specific functions. Indeed, there is abundant evidence that members of this family interact with glycoconjugates on or around cells and influence adhesion, migration, chemotaxis, proliferation, apoptosis, and neurite elongation (Barondes et al., 1994a; Puche et al., 1996; Hughes, 1997; Various authors, 1997; Matsumoto et al., 1998).

Even a single galectin can apparently affect cells in a variety of ways depending on the cell type and circumstances. For instance, galectin-1 can either stimulate or inhibit cell proliferation (Wells and Mallucci, 1991; Adams et al., 1996; Yamaoka et al., 1996) and can either stimulate or inhibit cell adhesion to extracellular matrix (Cooper et al., 1991; Van Den Brule et al., 1995). There is also evidence that galectins can simultaneously have distinct intracellular and extracellular functions. For instance, both galectin-1 and galectin-3 have been implicated in pre-mRNA splicing (Dagher et al., 1995; Vyakarnam et al., 1997).

Several recent studies have focused attention on possible galectin functions in regulating immune responses. For example, it has been found that galectin-1 or galectin-9 can induce apoptosis of activated T-cells by binding to cell surface oligosaccharides (Perillo et al., 1995; Wada et al., 1997; Allione et al., 1998; Vespa et al., 1998; Rabinovich et al., 1998; Novelli et al., 1999; ), galectin-3 can activate neutrophils (Yamaoka et al., 1995; Karlsson et al., 1998), and galectin-9 is a potent and specific chemoattractant for eosinophils (Matsumoto et al., 1998).

Another approach to study galectin function is to knock-out expression of individual galectin genes. Such mice lacking galectin-1 have so far been shown to have intriguing deficits in olfactory axon pathfinding (Puche et al., 1996). Mice lacking galectin-3 have so far been shown to have abnormalities in neutrophil accumulation during inflammation (Colnot et al., 1998). Although this approach can fail to detect normal biological functions of the missing protein, apparently because many functions can be performed by alternative or redundant systems, these initial positive results are very encouraging for further analysis of these and mice engineered to eliminate other galectin family members.

Acknowledgments

This work was supported in part by Grant R01-HL56199 from the USPHS to D.N.W.C.

References

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1To whom correspondence should be addressed
2Modified from the comment attributed to Abraham Lincoln, "God must love common people; He made so many of them."

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H. Walzel, A. A. Fahmi, M. A. Eldesouky, E. F. Abou-Eladab, G. Waitz, J. Brock, and M. Tiedge
Effects of N-glycan processing inhibitors on signaling events and induction of apoptosis in galectin-1-stimulated Jurkat T lymphocytes
Glycobiology, December 1, 2006; 16(12): 1262 - 1271.
[Abstract] [Full Text] [PDF]

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L. Kohatsu, D. K. Hsu, A. G. Jegalian, F.-T. Liu, and L. G. Baum
Galectin-3 Induces Death of Candida Species Expressing Specific beta-1,2-Linked Mannans
J. Immunol., October 1, 2006; 177(7): 4718 - 4726.
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 BloodHome page
P. V. Cabrera, M. Amano, J. Mitoma, J. Chan, J. Said, M. Fukuda, and L. G. Baum
Haploinsufficiency of C2GnT-I glycosyltransferase renders T lymphoma cells resistant to cell death
Blood, October 1, 2006; 108(7): 2399 - 2406.
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 GlycobiologyHome page
H. Stalz, U. Roth, D. Schleuder, M. Macht, S. Haebel, K. Strupat, J. Peter-Katalinic, and F.-G. Hanisch
The Geodia cydonium galectin exhibits prototype and chimera-type characteristics and a unique sequence polymorphism within its carbohydrate recognition domain
Glycobiology, May 1, 2006; 16(5): 402 - 414.
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 GlycobiologyHome page
G. A. Rabinovich, A. Cumashi, G. A. Bianco, D. Ciavardelli, I. Iurisci, M. D'Egidio, E. Piccolo, N. Tinari, N. Nifantiev, and S. Iacobelli
Synthetic lactulose amines: novel class of anticancer agents that induce tumor-cell apoptosis and inhibit galectin-mediated homotypic cell aggregation and endothelial cell morphogenesis
Glycobiology, March 1, 2006; 16(3): 210 - 220.
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M. Baba, J. Wada, J. Eguchi, I. Hashimoto, T. Okada, A. Yasuhara, K. Shikata, Y. S. Kanwar, and H. Makino
Galectin-9 Inhibits Glomerular Hypertrophy in db/db Diabetic Mice via Cell-Cycle-Dependent Mechanisms
J. Am. Soc. Nephrol., November 1, 2005; 16(11): 3222 - 3234.
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S. Karmakar, R. D. Cummings, and R. P. McEver
Contributions of Ca2+ to Galectin-1-induced Exposure of Phosphatidylserine on Activated Neutrophils
J. Biol. Chem., August 5, 2005; 280(31): 28623 - 28631.
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 GlycobiologyHome page
H. Shoji, K. Ikenaka, S.-i. Nakakita, K. Hayama, J. Hirabayashi, Y. Arata, K.-i. Kasai, N. Nishi, and T. Nakamura
Xenopus galectin-VIIa binds N-glycans of members of the cortical granule lectin family (xCGL and xCGL2)
Glycobiology, July 1, 2005; 15(7): 709 - 720.
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A. Leppanen, S. Stowell, O. Blixt, and R. D. Cummings
Dimeric Galectin-1 Binds with High Affinity to {alpha}2,3-Sialylated and Non-sialylated Terminal N-Acetyllactosamine Units on Surface-bound Extended Glycans
J. Biol. Chem., February 18, 2005; 280(7): 5549 - 5562.
[Abstract] [Full Text] [PDF]

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 GlycobiologyHome page
H. Walzel, J. Brock, R. Pohland, J. Vanselow, W. Tomek, F. Schneider, and U. Tiemann
Effects of galectin-1 on regulation of progesterone production in granulosa cells from pig ovaries in vitro
Glycobiology, October 1, 2004; 14(10): 871 - 881.
[Abstract] [Full Text] [PDF]

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 GlycobiologyHome page
N. Ahmad, H.-J. Gabius, S. Sabesan, S. Oscarson, and C. F. Brewer
Thermodynamic binding studies of bivalent oligosaccharides to galectin-1, galectin-3, and the carbohydrate recognition domain of galectin-3
Glycobiology, September 1, 2004; 14(9): 817 - 825.
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 Cancer Res.Home page
S. Ueda, I. Kuwabara, and F.-T. Liu
Suppression of Tumor Growth by Galectin-7 Gene Transfer
Cancer Res., August 15, 2004; 64(16): 5672 - 5676.
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 GlycobiologyHome page
S. Morris, N. Ahmad, S. Andre, H. Kaltner, H.-J. Gabius, M. Brenowitz, and F. Brewer
Quaternary solution structures of galectins-1, -3, and -7
Glycobiology, March 1, 2004; 14(3): 293 - 300.
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F. Dalle, T. Jouault, P. A. Trinel, J. Esnault, J. M. Mallet, P. d'Athis, D. Poulain, and A. Bonnin
{beta}-1,2- and {alpha}-1,2-Linked Oligomannosides Mediate Adherence of Candida albicans Blastospores to Human Enterocytes In Vitro
Infect. Immun., December 1, 2003; 71(12): 7061 - 7068.
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T. Fukumori, Y. Takenaka, T. Yoshii, H.-R. C. Kim, V. Hogan, H. Inohara, S. Kagawa, and A. Raz
CD29 and CD7 Mediate Galectin-3-Induced Type II T-Cell Apoptosis
Cancer Res., December 1, 2003; 63(23): 8302 - 8311.
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D. A. Carlow, M. J. Williams, and H. J. Ziltener
Modulation of O-Glycans and N-Glycans on Murine CD8 T Cells Fails to Alter Annexin V Ligand Induction by Galectin 1
J. Immunol., November 15, 2003; 171(10): 5100 - 5106.
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M. Dias-Baruffi, H. Zhu, M. Cho, S. Karmakar, R. P. McEver, and R. D. Cummings
Dimeric Galectin-1 Induces Surface Exposure of Phosphatidylserine and Phagocytic Recognition of Leukocytes without Inducing Apoptosis
J. Biol. Chem., October 17, 2003; 278(42): 41282 - 41293.
[Abstract] [Full Text] [PDF]

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 GlycobiologyHome page
H. Ideo, A. Seko, I. Ishizuka, and K. Yamashita
The N-terminal carbohydrate recognition domain of galectin-8 recognizes specific glycosphingolipids with high affinity
Glycobiology, October 1, 2003; 13(10): 713 - 723.
[Abstract] [Full Text] [PDF]

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I. Pelletier, T. Hashidate, T. Urashima, N. Nishi, T. Nakamura, M. Futai, Y. Arata, K.-i. Kasai, M. Hirashima, J. Hirabayashi, et al.
Specific Recognition of Leishmania major Poly-{beta}-galactosyl Epitopes by Galectin-9: POSSIBLE IMPLICATION OF GALECTIN-9 IN INTERACTION BETWEEN L. MAJOR AND HOST CELLS
J. Biol. Chem., June 13, 2003; 278(25): 22223 - 22230.
[Abstract] [Full Text] [PDF]

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 Integr. Comp. Biol.Home page
M. S. Quesenberry, H. Ahmed, M. T. Elola, N. O'Leary, and G. R. Vasta
Diverse Lectin Repertoires in Tunicates Mediate Broad Recognition and Effector Innate Immune Responses
Integr. Comp. Biol., April 1, 2003; 43(2): 323 - 330.
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H. Shoji, N. Nishi, M. Hirashima, and T. Nakamura
Characterization of the Xenopus Galectin Family. THREE STRUCTURALLY DIFFERENT TYPES AS IN MAMMALS AND REGULATED EXPRESSION DURING EMBRYOGENESIS
J. Biol. Chem., March 28, 2003; 278(14): 12285 - 12293.
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A. M. Moody, S. J. North, B. Reinhold, S. J. Van Dyken, M. E. Rogers, M. Panico, A. Dell, H. R. Morris, J. D. Marth, and E. L. Reinherz
Sialic Acid Capping of CD8beta Core 1-O-Glycans Controls Thymocyte-Major Histocompatibility Complex Class I Interaction
J. Biol. Chem., February 21, 2003; 278(9): 7240 - 7246.
[Abstract] [Full Text] [PDF]

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F. Dromer, R. Chevalier, B. Sendid, L. Improvisi, T. Jouault, R. Robert, J. M. Mallet, and D. Poulain
Synthetic Analogues of {beta}-1,2 Oligomannosides Prevent Intestinal Colonization by the Pathogenic Yeast Candida albicans
Antimicrob. Agents Chemother., December 1, 2002; 46(12): 3869 - 3876.
[Abstract] [Full Text] [PDF]

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 Protein Eng Des SelHome page
T. K. Mandal and C. Mukhopadhyay
Binding free energy calculations of galectin-3-ligand interactions
Protein Eng. Des. Sel., December 1, 2002; 15(12): 979 - 986.
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 GlycobiologyHome page
J. D. Hernandez and L. G. Baum
Ah, sweet mystery of death! Galectins and control of cell fate
Glycobiology, October 1, 2002; 12(10): 127R - 136R.
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 Proc. Natl. Acad. Sci. USAHome page
L. G. Ellies, D. Ditto, G. G. Levy, M. Wahrenbrock, D. Ginsburg, A. Varki, D. T. Le, and J. D. Marth
Sialyltransferase ST3Gal-IV operates as a dominant modifier of hemostasis by concealing asialoglycoprotein receptor ligands
PNAS, July 23, 2002; 99(15): 10042 - 10047.
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I. Pelletier and S. Sato
Specific Recognition and Cleavage of Galectin-3 by Leishmania major through Species-specific Polygalactose Epitope
J. Biol. Chem., May 10, 2002; 277(20): 17663 - 17670.
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J. Almkvist, C. Dahlgren, H. Leffler, and A. Karlsson
Activation of the Neutrophil Nicotinamide Adenine Dinucleotide Phosphate Oxidase by Galectin-1
J. Immunol., April 15, 2002; 168(8): 4034 - 4041.
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K. E. Pace, T. Lebestky, T. Hummel, P. Arnoux, K. Kwan, and L. G. Baum
Characterization of a Novel Drosophila melanogaster Galectin. EXPRESSION IN DEVELOPING IMMUNE, NEURAL, AND MUSCLE TISSUES
J. Biol. Chem., April 5, 2002; 277(15): 13091 - 13098.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
S. Yu, N. Kojima, S.-i. Hakomori, S. Kudo, S. Inoue, and Y. Inoue
Binding of rainbow trout sperm to egg is mediated by strong carbohydrate-to-carbohydrate interaction between (KDN)GM3 (deaminated neuraminyl ganglioside) and Gg3-like epitope
PNAS, March 5, 2002; 99(5): 2854 - 2859.
[Abstract] [Full Text] [PDF]

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 GlycobiologyHome page
H. Shoji, N. Nishi, M. Hirashima, and T. Nakamura
Purification and cDNA cloning of Xenopus liver galectins and their expression
Glycobiology, March 1, 2002; 12(3): 163 - 172.
[Abstract] [Full Text] [PDF]

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 GlycobiologyHome page
H. Ideo, A. Seko, T. Ohkura, K. L. Matta, and K. Yamashita
High-affinity binding of recombinant human galectin-4 to SO3-->3Gal{beta}1->3GalNAc pyranoside
Glycobiology, March 1, 2002; 12(3): 199 - 208.
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S. Sato, N. Ouellet, I. Pelletier, M. Simard, A. Rancourt, and M. G. Bergeron
Role of Galectin-3 as an Adhesion Molecule for Neutrophil Extravasation During Streptococcal Pneumonia
J. Immunol., February 15, 2002; 168(4): 1813 - 1822.
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 GlycobiologyHome page
C. M. West, H. van der Wel, and E. A. Gaucher
Complex glycosylation of Skp1 in Dictyostelium: implications for the modification of other eukaryotic cytoplasmic and nuclear proteins
Glycobiology, February 1, 2002; 12(2): 17R - 27R.
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I. Kuwabara, Y. Kuwabara, R.-Y. Yang, M. Schuler, D. R. Green, B. L. Zuraw, D. K. Hsu, and F.-T. Liu
Galectin-7 (PIG1) Exhibits Pro-apoptotic Function through JNK Activation and Mitochondrial Cytochrome c Release
J. Biol. Chem., January 25, 2002; 277(5): 3487 - 3497.
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K. Goldring, G. E. Jones, R. Thiagarajah, and D. J. Watt
The effect of galectin-1 on the differentiation of fibroblasts and myoblasts in vitro
J. Cell Sci., January 15, 2002; 115(2): 355 - 366.
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 DevelopmentHome page
P. M. Timmons, P. W. J. Rigby, and F. Poirier
The murine seminiferous epithelial cycle is pre-figured in the Sertoli cells of the embryonic testis
Development, January 2, 2002; 129(3): 635 - 647.
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 GlycobiologyHome page
R. B. Dodd and K. Drickamer
Lectin-like proteins in model organisms: implications for evolution of carbohydrate-binding activity
Glycobiology, May 1, 2001; 11(5): 71R - 79R.
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 GlycobiologyHome page
D. Solis, M. I.F. Lopez-Lucendo, S. Leon, J. Varela, and T. Diaz-Maurino
Description of a monomeric prototype galectin from the lizard Podarcis hispanica
Glycobiology, December 1, 2000; 10(12): 1325 - 1331.
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H. Sano, D. K. Hsu, L. Yu, J. R. Apgar, I. Kuwabara, T. Yamanaka, M. Hirashima, and F.-T. Liu
Human Galectin-3 Is a Novel Chemoattractant for Monocytes and Macrophages
J. Immunol., August 15, 2000; 165(4): 2156 - 2164.
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 GlycobiologyHome page
A. Seppo and M. Tiemeyer
Function and structure of Drosophila glycans
Glycobiology, April 1, 2000; 10(8): 751 - 760.
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P. B. Miarons and M. Fresno
Lectins from Tropical Sponges. PURIFICATION AND CHARACTERIZATION OF LECTINS FROM GENUS APLYSINA
J. Biol. Chem., September 15, 2000; 275(38): 29283 - 29289.
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Y. Arata, J. Hirabayashi, and K.-i. Kasai
Sugar Binding Properties of the Two Lectin Domains of the Tandem Repeat-type Galectin LEC-1 (N32) of Caenorhabditis elegans. DETAILED ANALYSIS BY AN IMPROVED FRONTAL AFFINITY CHROMATOGRAPHY METHOD
J. Biol. Chem., January 26, 2001; 276(5): 3068 - 3077.
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R.-Y. Yang, D. K. Hsu, L. Yu, J. Ni, and F.-T. Liu
Cell Cycle Regulation by Galectin-12, a New Member of the Galectin Superfamily
J. Biol. Chem., June 1, 2001; 276(23): 20252 - 20260.
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